Regulation of abscisic acid receptor mRNA stability: involvement of microRNA5628 in PYL6 transcript decay

João G P Vieira; Gustavo T Duarte; Carlos H Barrera-Rojas; Cleverson C Matiolli; Américo J C Viana; Raphael de A Campos; Lucas E D Canesin; Renato Vicentini; Fabio T S Nogueira; Michel Vincentz

doi:10.1093/plphys/kiae663

Regulation of abscisic acid receptor mRNA stability: involvement of microRNA5628 in PYL6 transcript decay

Plant Physiol. 2024 Dec 21:kiae663. doi: 10.1093/plphys/kiae663. Online ahead of print.

Affiliations

¹ Laboratory of Plant Genetics, Center for Molecular Biology and Genetic Engineering, University of Campinas, 13083-875, Campinas, São Paulo, Brazil.
² Belgian Nuclear Research Centre (SCK CEN), Unit for Biosphere Impact Studies, Boeretang 200, 2400, Mol, Belgium.
³ Laboratory of Molecular Genetics of Plant Development, Department of Biological Sciences, Escola Superior de Agricultura 'Luiz de Queiroz', University of Sao Paulo, Piracicaba, Sao Paulo, 13418-900, Brazil.
⁴ Genomics for Climate Change Research Group, Center for Molecular Biology and Genetic Engineering, University of Campinas, 13083-875, Campinas, São Paulo, Brazil.
⁵ Systems Biology Laboratory, Department of Plant Genetics and Breeding, University of Campinas, 13083-862, Campinas, São Paulo, Brazil.

PMID: 39707902
DOI: 10.1093/plphys/kiae663

Abstract

Phytohormone signaling is fine-tuned by regulatory feedback loops. The phytohormone abscisic acid (ABA) plays key roles in plant development and abiotic stress tolerance. PYRABACTIN RESISTENCE 1/PYR1-LIKE/REGULATORY COMPONENT OF ABA RECEPTOR (PYR/PYL/RCAR) receptors sense ABA, and in turn, ABA represses their expression. Conversely, ABA induces expression of type 2C PROTEIN PHOSPHATASES (PP2C) genes, which negatively regulate the ABA signaling pathway. This regulatory feedback scheme is likely important for modulating ABA signaling. Here, we provide insight into the mechanisms underlying the ABA-induced repression of PYR/PYL/RCAR expression in Arabidopsis (Arabidopsis thaliana). ABA time course analyses revealed strong and sustained repression of PYR/PYL/RCARs, suggesting that receptor gene regulation is an important step in resetting the ABA signaling pathway. Cordycepin-induced transcription inhibition showed that PYL1/4/5/6 mRNA destabilization is involved in the ABA-induced repression of these genes. Furthermore, genetic evidence indicated that decapping may play a role in PYL4/5/6 mRNA decay. We also provide evidence that the Arabidopsis-specific microRNA5628 (miR5628), which is transiently induced by the ABA core signaling pathway, guides PYL6 transcript cleavage in response to ABA. After cleavage, the resulting 5'- and 3'-cleaved fragments of PYL6 mRNA may be degraded by the XRN4 exoribonuclease. miR5628 is an evolutionary novelty that may enhance PYL6 mRNA degradation, along with decapping and XRN4 activity. Thus, regulating the stability of PYR/PYL/RCAR transcripts maintains ABA signaling homeostasis.

Keywords: ABA signaling; Abscisic acid; XRN4; decapping and exoribonuclease activity; homeostasis; mRNA decay; microRNA; negative feedback.

© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.